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Colorectal cancer among Koreans living in South Korea versus California: Incidence, mortality and screening rates Prof. So Yeon Ryu, Chosun University Medical School, Gwangju, Korea, Republic of Dr. Catherine M. Crespi, and UCLA School of Public Health, Biostatistics, UCLA Pub Hlth-Biostat, BOX 951772, Los Angeles, 90095-1772 United Kingdom Prof. Annette E Maxwell, DrPH UCLA, Health Policy and Management, Los Angeles, United States Annette E Maxwell: [email protected] Abstract Objectives—This study compared trends in colorectal cancer (CRC) incidence and mortality rates among Koreans in South Korea and Korean Americans and non-Hispanic whites in California between 1999 and 2009, and examined CRC screening rates and socio-demographic correlates of CRC screening in the two Korean populations. Design—Age-standardized CRC incidence and mortality rates of Koreans in South Korea and Korean Americans and non-Hispanic whites in California for the years 1999–2009 were obtained from annual reports of cancer statistics and modeled using joinpoint regression. Using 2009 data from the Korean National Health and Nutrition Examination Survey and the California Health Interview Survey, we estimated and compared CRC screening rates and test modalities. We used multiple logistic regression to examine socio-demographic correlates of completion of CRC screening according to the guidelines among the two Korean populations. Results—CRC incidence and mortality rates among South Koreans increased during 1999–2009 but more slowly during the late 2000s. In California, CRC incidence increased among Korean American females but decreased among non-Hispanic whites. About 37% of South Koreans and 60% of Korean Americans reported completion of CRC screening according to guidelines in 2009. Among South Koreans, married status, higher income and private health insurance were associated with CRC screening, adjusting for other factors. Among Korean Americans, having health insurance was associated with CRC screening. Conclusion—Despite almost identical CRC screening guidelines in South Korea and the US and substantially higher screening rates among Korean Americans as compared to South Koreans, disparities remain in both populations with respect to CRC statistics. Thus, efforts to promote primary and secondary prevention of CRC in both Korean populations are critically important in both countries. Correspondence to: Annette E Maxwell, [email protected]. HHS Public Access Author manuscript Ethn Health. Author manuscript; available in PMC 2015 August 01. Published in final edited form as: Ethn Health. 2014 August ; 19(4): 406–423. doi:10.1080/13557858.2013.801404. Author Manuscript Author Manuscript Author Manuscript Author Manuscript

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Page 1: Centers for Disease Control and Prevention - HHS …Colorectal cancer among Koreans living in South Korea versus California: Incidence, mortality and screening rates Prof. So Yeon

Colorectal cancer among Koreans living in South Korea versus California: Incidence, mortality and screening rates

Prof. So Yeon Ryu,Chosun University Medical School, Gwangju, Korea, Republic of

Dr. Catherine M. Crespi, andUCLA School of Public Health, Biostatistics, UCLA Pub Hlth-Biostat, BOX 951772, Los Angeles, 90095-1772 United Kingdom

Prof. Annette E Maxwell, DrPHUCLA, Health Policy and Management, Los Angeles, United States

Annette E Maxwell: [email protected]

Abstract

Objectives—This study compared trends in colorectal cancer (CRC) incidence and mortality

rates among Koreans in South Korea and Korean Americans and non-Hispanic whites in

California between 1999 and 2009, and examined CRC screening rates and socio-demographic

correlates of CRC screening in the two Korean populations.

Design—Age-standardized CRC incidence and mortality rates of Koreans in South Korea and

Korean Americans and non-Hispanic whites in California for the years 1999–2009 were obtained

from annual reports of cancer statistics and modeled using joinpoint regression. Using 2009 data

from the Korean National Health and Nutrition Examination Survey and the California Health

Interview Survey, we estimated and compared CRC screening rates and test modalities. We used

multiple logistic regression to examine socio-demographic correlates of completion of CRC

screening according to the guidelines among the two Korean populations.

Results—CRC incidence and mortality rates among South Koreans increased during 1999–2009

but more slowly during the late 2000s. In California, CRC incidence increased among Korean

American females but decreased among non-Hispanic whites. About 37% of South Koreans and

60% of Korean Americans reported completion of CRC screening according to guidelines in 2009.

Among South Koreans, married status, higher income and private health insurance were

associated with CRC screening, adjusting for other factors. Among Korean Americans, having

health insurance was associated with CRC screening.

Conclusion—Despite almost identical CRC screening guidelines in South Korea and the US and

substantially higher screening rates among Korean Americans as compared to South Koreans,

disparities remain in both populations with respect to CRC statistics. Thus, efforts to promote

primary and secondary prevention of CRC in both Korean populations are critically important in

both countries.

Correspondence to: Annette E Maxwell, [email protected].

HHS Public AccessAuthor manuscriptEthn Health. Author manuscript; available in PMC 2015 August 01.

Published in final edited form as:Ethn Health. 2014 August ; 19(4): 406–423. doi:10.1080/13557858.2013.801404.

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Keywords

colorectal cancer; incidence; mortality; screening; socio-economic disparities; South Korea; Korean Americans; trends

Introduction

Globally, colorectal cancer (CRC) is the second and third most common cancer in women

and men, respectively (IARC. 2010). In recent years, CRC incidence and mortality rates

have generally increased in economically developing countries while in economically

developed countries rates have stabilized or are declining (Center el al. 2009). CRC

screening has been demonstrated to reduce both the incidence of and mortality from CRC

(Newcomb et al. 1992, Selby et al. 1992, Selby et al. 1993, Hardcastle et al. 1996, Kronburg

et al. 2004, Mandel et al., 1999, Mandel et al. 2000, Atkin et al. 2010, Edwards et al. 2010,

Segnan et al. 2011, Schoen et al. 2012). Declines in CRC death rates in the US are consistent

with a relatively large contribution from screening and a smaller impact of risk factor

reductions and improved treatments (Edwards, et a. 2010). Based on the benefits of

screening, the US Preventive Services Task Force and the Asia Pacific Working Group on

Colorectal Cancer have recommended CRC screening for average-risk persons aged 50

years or older using annual high sensitivity fecal occult blood test (FOBT) or fecal

immunochemical test (FIT), flexible sigmoidoscopy every 5 years, or colonoscopy every 10

years (U.S. Preventive Services Task Force 2002, Sung et al. 2008).

In the US, CRC screening was introduced in the 1970s and 1980s, and gradual increases in

utilization of screening have continued since the late 1980s, with marked changes in

screening methods including the declining use of FOBT and increasing use of endoscopic

procedures such as colonoscopy (Seeff et al. 2004, Meissner et al. 2006). Most health

insurance includes coverage for routine CRC screening. The history of CRC screening in

South Korea is relatively short compared to the US. In 2002, South Korea developed

guidelines for CRC screening in average-risk adults, and the government introduced

nationwide CRC screening as part of the National Cancer Screening Program (NCSP) in

2004 (Choi et al. 2010). Currently, in Korea, both government-organized and opportunistic

CRC screening is available. Free annual FOBT is provided by the government as part of the

NCSP for those with an income level below the 50th percentile, and participants with a

positive result can undergo additional screening such as colonoscopy and double-contrast

barium enema test (DCBE) at low cost. Those with an income level above the 50th

percentile can obtain opportunistic screening and have to pay the full cost of screening out

of pocket, whether it is FOBT, flexible sigmoidoscopy or colonoscopy (Yoo. 2008). South

Koreans with higher levels of income often purchase private health insurance to supplement

coverage under the mandatory National Health Insurance System. However, private health

insurance generally does not include coverage for CRC screening (Myong et al. 2012).

Despite the evidence suggesting that screening reduces CRC incidence and mortality,

participation in CRC screening is low, especially among South Koreans and Korean

Americans (Lemon et al. 2001, Maxwell and Crespi, 2009, Choi et al. 2010, Homayoon et

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al. 2012). Demographic characteristics, socioeconomic status, access to health care services

and acculturation have been found to be associated with utilization of CRC screening in

various populations (Ioannou et al. 2003, Wong et al. 2005, Kandula et al. 2006, Choi et al.

2010, Maxwell et al. 2010, Lee et al. 2011, Myong et al. 2012). Although South Koreans

and Korean Americans share genetic and cultural characteristics, they may experience

differences with respect to lifestyle, environment and access to health care that affect their

rates of CRC screening, incidence and mortality. Comparison of the health status of

migrants and host country non-migrants provides an opportunity to separate the influences

of genetic and environmental factors (McKay et al., 2003). For example, studies have shown

that people who migrate from low-risk to high-risk countries generally experience a gradual

increase in cancer incidence (Stewart and Kleihues, 2003), and such studies have helped in

understanding the relative contributions of genetic and environmental risk factors for cancer.

However, relatively little is known about comparative trends in CRC incidence and

mortality rates and about the factors related to participation in CRC screening among

Koreans in South Korea and the US.

This study analyzed large scale, population-based data with three objectives. The first

objective was to compare trends in CRC incidence and mortality rates among Koreans in

South Korea and Korean Americans and non-Hispanic whites in California between 1999

and 2009. The second objective was to compare the proportions of Koreans in South Korea

and Korean Americans in California that reported receipt of any CRC screening (lifetime

CRC screening) and CRC screening according to the guidelines (up-to-date CRC screening).

Finally we sought to identify socio-demographic disparities in CRC screening according to

the guidelines among Koreans in South Korea and Korean Americans in California. We

analyzed data from Korean Americans in California because one third of all Korean

Americans live in California (Hoeffel et al 2012) and the California Health Interview Survey

is the largest population-based health survey in the United States that is conducted in Korean

language and has a large number of Korean American respondents.

Methods

Age-standardized CRC incidence and mortality rates

Age-standardized CRC incidence and mortality rates by gender were obtained from public

data sources in South Korea and California. Rates between 1999 and 2009 in South Korea

were obtained from annual reports of cancer statistics published by the Korea Cancer

Registry and National Cancer Center (Korea Central Cancer Registry 2011), and statistics on

cause of death were obtained from Korean Statistical Information Service of Statistics Korea

(Korean Statistical Information Service 2012). For Korean Americans and non-Hispanic

whites in California, these statistics were obtained from the California Cancer Registry and

California Department of Public Health Death Statistical Master files for 1988–2009. These

data sources provided age-standardized rates per 100,000 adults. Rates for Korean

Americans and non-Hispanic whites in California used the year 2000 US standard

population, and rates for Koreans in South Korea used the year 2000 Korean standard

population for incidence and year 2005 Korean standard population for mortality. Since raw

data with which to standardize all rates to the same population were not available, the results

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support comparison of trends across countries but not comparison of absolute rates across

countries.

Analyses of participation in CRC screening

1) Data—Population-based survey data from the publicly available 2009 Korean National

Health and Nutrition Examination Survey (KNHANES, for South Koreans) and 2009

California Health Interview Survey (CHIS, for Korean Americans) were used for analysis of

participation in CRC screening.

The KNHANES is a nationwide, population-based, cross-sectional health survey designed to

assess the health and nutritional status of the non-institutionalized civilian population of

South Korea, conducted by the Korea Center for Diseases Control and Prevention. After the

first KNHANES was performed in 1998, the fourth round of surveys was conducted in

2007–2009. The present study used data obtained in 2009, which was the 3rd year of the

ongoing KNHANES IV. The 2009 KNHANES used a stratified multistage cluster

probability sampling design. The sampling frame was derived from the 2005 population and

housing census. For 2009 KNHANES, 200 sampling units were randomly selected from the

264,186 primary sampling units encompassing the target population in Korea, and 20–23

households were selected from each primary sampling unit to yield 4600 households. The

field survey was conducted by specially trained interviewers at mobile centers and in the

participants’ households. Surveys were completed by 10,533 participants (participation rate

82.8%; Ministry of Health Welfare & Korea Center of Disease Control and Prevention

2010).

The CHIS, a biennial statewide survey conducted in California, is the largest state health

survey in the US. The 2009 CHIS employed a multistage sampling design. Within each of

56 geographic strata, random-digit-dial that included telephone numbers assigned to both

landline and cellular service was used to sample households; within each household, one

adult (age 18 and over) was randomly selected for a telephone interview. Korean and

Vietnamese Americans were oversampled to increase the precision of estimates for these

groups. Interviews were conducted in English, Spanish, Cantonese, Mandarin, Vietnamese

and Korean. The 2009 CHIS interviewed a total of 47,614 adults. We identified respondents

as Korean American based on the Asian group definitions (CHIS 2011).

The samples for this study were restricted to individuals aged 50 years and older because the

guidelines in each nation recommend that CRC screening begin at age 50. The final sample

sizes of South Koreans and Korean Americans in this study were 3,532 and 519,

respectively.

2) Variables—All variables were based on self report. The outcome variables were up-to-

date CRC screening, defined as participation in CRC screening according to the guidelines

of the respondent’s country, which were receipt of either FOBT within the past year, flexible

sigmoidoscopy within the past 5 years or colonoscopy within the past 10 years; for South

Koreans, the guidelines and our definition also included DCBE within the past 5 years (U.S.

Preventive Services Task Force 2002, Sung et al. 2008), and life-time screening, defined as

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ever receiving an FOBT, sigmoidoscopy or colonoscopy; for South Koreans, DCBE was

also included. DCBE was not assessed in CHIS.

Socio-demographic variables included age, gender, marital status, educational attainment,

household income and place of residence. Marital status was categorized as living with a

partner or not, and educational attainment was classified as less than high school or high

school graduate and over. Tertiles of household income were defined based on the income

distribution within each entire original sample prior to restriction to age 50 years and older.

Place of residence was categorized as urban or rural based on variables provided in the two

data sets. For KNHANES, the variable was based on Korean place name conventions that

distinguish urban and rural areas. In CHIS, the classifications of the Federal Office of Rural

Health Policy were used, whereby counties are classified based on the Office of

Management and Budget designations of metropolitan and non-metropolitan areas but

certain census tracts within these counties are designated as rural to account for rural areas

within large urban counties. English speaking ability was used as a measure of acculturation

in Korean Americans. The 3 response categories were “Only English”, “Very well/ well”

and “Not well/ not at all”, which we dichotomized as only English/very well/well and not

well/not at all.

For the California sample, health insurance, which generally covers the cost of CRC

screening, was dichotomized as “yes” and “no”. This dichotomy was not relevant for the

South Korean sample because all South Koreans are insured by the Korean National Health

Insurance or medical aid programs. Instead, for the KNHANES sample, a dichotomous

variable for private health insurance was used; however, such insurance generally does not

cover CRC screening.

3) Statistical analysis—Trends in gender-specific CRC incidence and mortality rates

were analyzed using joinpoint models (Kim et al. 2000) fit using the Joinpoint Regression

Program Version 4.0.1 (January 9, 2013), available at http://surveillance.cancer.gov/

joinpoint/. This model allows for changepoints or “joinpoint” in trend data, at which there is

a change in rates; it fits the simplest joinpoint model that the data allow as determined using

a permutations test and estimates the average annual percent change (AAPC) in rate along

each interval between joinpoints.

Other statistical analyses were carried out using SAS statistical software (version 9.2, SAS

institute Inc, NC). Survey weights were used in all analyses. Estimated percentages for

socio-demographic variables and for lifetime and up-to-date CRC screening, as well as type

of test, were obtained using the surveyfreq procedure. Multiple logistic regression was used

to estimate the odds ratio (OR) and 95% confidence intervals (CI) for the association

between up-to-date CRC screening and socio-demographic variables using the

surveylogistic procedure, and repeated for lifetime CRC screening. For all tests of statistical

significance, p<0.05 was used.

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Results

Table 1 provides estimated average annual percent change in age-standardized CRC

incidence and mortality among Koreans in South Korea and Korean Americans and non-

Hispanic whites in California between 1999 and 2009. The age-standardized rates are

presented in Figure 1. The data upon which the figure is based are provided in the appendix.

Among South Koreans, the CRC incidence rate increased in both sexes during 1999–2009,

but with a slowing in the rate of increase around 2005–2006 (from AAPC=8.1 to AAPC=4.4

in males; from AAPC=6.4 to AAPC=3.0 in females, all P<0.05). CRC mortality rates

increased in both sexes during 1999–2003 (through 2004 for females), then leveled off such

that there was no significant change in rates in the more recent years (from AAPC=5.7 to

AAPC=−0.1 in males; from AAPC=2.9 to AAPC=−1.0 in females; P<0.05 only for first

AAPC for each gender). Incidence and mortality rates were higher among males than

females (P<0.05).

Among Korean Americans in California, the CRC incidence rate increased significantly

among females during 1999–2009 (AAPC=2.7, P<0.05); among males, no significant

change in incidence was detected (AAPC=1.8, P>0.05). Both sexes had estimated decreases

in mortality rates that were not significantly different from no change (AAPC=−1.3 for

males, AAPC=−1.2 for females, both P>0.05).

Among non-Hispanic whites in California, CRC incidence rates decreased significantly

among both sexes (AAPC=−2.5 for males, AAPC=−1.7 for females, both P<0.05); CRC

mortality rates also decreased significantly (AAPC=−2.5 for males, AAPC=−2.2 for

females, both P<0.05).

Table 2 presents socio-demographic characteristics of the two study populations, Koreans in

South Korea and Korean Americans in California aged 50 or older, based on the 2009

population-based survey data. The Korean American population was older, more likely to be

female, more highly educated, more likely to be in the middle income tertile and more likely

to live in urban areas than the South Korean population. English proficiency levels were low

among the Korean Americans, with 70% speaking English not well or not at all.

Lifetime CRC screening rates were 42.9% among South Koreans and 70.2% among Korean

Americans (data not shown). As shown in Figure 2, up-to-date screening rates were 37.1%

among South Koreans and 60.4% among Korean Americans. In comparison, 71.8% of non-

Hispanic whites residing in California reported up-to-date CRC screening (data not shown).

Among South Koreans with up-to-date CRC screening, about half reported receipt of an

FOBT (19.6% of the total sample) and half receipt of colonoscopy (19.2%); in contrast,

most Korean Americans with up-to-date CRC screening reported receipt of a colonoscopy

(50.2% of the total sample), followed by FOBT (18.9%). Among South Koreans with the

lowest income level in this study, the most common CRC screening method was FOBT

(18%), followed by colonoscopy (13%). Among South Koreans with the highest income

level, the most common CRC screening method was colonoscopy (28%), followed by FOBT

(21%; data not shown).

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Bivariate analyses examining the association between up-to-date CRC screening and socio-

demographic variables are presented in Table 3. South Koreans who were male, less than 65

years of age, married, with higher levels of education and income, living in an urban area

and with private health insurance were more likely to report up-to-date CRC screening.

Among Korean Americans, the only variable that was significantly associated with up-to-

date CRC screening was having health insurance. Patterns of association were similar for

lifetime screening for both groups (data not shown).

Table 4 shows the results of multiple logistic regression analysis for the outcome of up-to-

date CRC screening among South Koreans and Korean Americans. Among South Koreans,

married status (OR=1.48, 95% CI=1.18–1.85), 3rd tertile of income (OR=1.34, 95%

CI=1.08–1.66) and private health insurance (OR=1.39, 95% CI=1.11–1.75) were associated

with up-to-date screening, controlling for other variables. Among Korean Americans, having

health insurance was the only statistically significant correlate of up-to-date CRC screening

(OR=2.61, 95% CI=1.04–6.55). Analysis using lifetime CRC screening as the outcome

yielded similar results (data not shown).

Discussion

Analyses that encompassed an earlier time period (Bates et al., 2010) found that CRC

incidence for Korean American men and women increased significantly between 1988 and

2007 (+3.6% per year for men, (+2.4% per year for women). When examining a more recent

time period and allowing for APC changepoints, we found that increases in CRC incidence

and mortality rates among Korean Americans in California were starting to level off

between 1999 and 2009. Our analyses also show improvements among South Koreans in

CRC incidence, starting in 2005/2006, and CRC mortality, starting in 2003/2004. However,

in both Korean populations, we did not observe the significant decreases in rates that are

found among non-Hispanic whites in California in the same time period. Thus, disparities in

CRC incidence and mortality remain.

Possible explanations for these disparities among South Koreans and Korean Americans in

California are increases in cancer risk factors due to adoption of a more westernized

lifestyle, including dietary changes, lack of physical activity and obesity (Wakai et al. 2006,

Han et al. 2011), combined with relatively recent adoption of CRC screening and low uptake

of screening. Although the US general population is also increasingly adopting an unhealthy

lifestyle as evidenced by the obesity epidemic, there has been a decline in CRC incidence

and mortality in the US population overall, which has been largely attributed to increased

utilization of CRC screening (Edwards et al. 2010). A comparison between the two

California samples points to the important influence of CRC screening utilization on CRC

incidence among non-Hispanic whites, who have lower CRC incidence rates than Korean

Americans despite higher obesity rates (Maxwell et al.2011). Due to a substantial increase in

CRC incidence among Korean Americans, their rates exceeded those of non-Hispanic

whites by the end of the study period. This trend is similar to the trend in breast cancer

incidence among Asian American women, which was traditionally very low but has

increased with change in lifestyle among groups with longer duration of residency in the

United States (Keegan et al. 2007). It is possible that CRC incidence and mortality rates will

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improve in the future as the preventive impacts of increased screening rates become

apparent. Nevertheless, our findings underscore the importance of monitoring trends to

identify at-risk populations that may require specialized programs to reduce their cancer

burden.

Our findings indicate that participation in CRC screening is less than optimal among Korean

Americans in California and even more so among Koreas in South Korea. However,

compared to a previous analysis of 2005 CHIS data (Maxwell and Crespi 2009), up-to-date

screening rates have increased remarkably among Korean Americans (from 29% in 2005 to

60.4% in 2009) and among non-Hispanic whites (from 59% to 71.8%). It has also been

reported that the up-to-date screening rate among South Koreans shows an increasing trend

(23% in 2005, 37% in 2008) (Choi et al. 2010). These findings may be due to public health

or educational policies and/or increased public awareness about CRC screening. It is

important to continue efforts to promote and provide CRC screening.

Screening by colonoscopy is recommended by many professional societies and has received

media attention as a most sensitive test (US. Preventive Service Task Force 2002). In South

Korea as well as the US, colonoscopy is much more costly than FOBT. Since 2004, the

Korean government and NCSP have provided free annual FOBT for low-income

individuals. Endoscopy is only provided for free to those whose FOBT results are positive.

Furthermore, the national health insurance program only reimburses colonoscopy for those

with symptoms or colorectal problems, not for routine screening (Yoo 2008). As described

above, use of colonoscopy versus FOBT varied with income level among Koreans in South

Korea, suggesting that out-of-pocket cost is an important determinant of the type of test

received. The increased utilization of colonoscopy versus FOBT among Korean Americans

may also be influenced by the type of test recommended by providers and personal

preferences.

Our results regarding determinants of CRC screening are consistent with previously

published studies indicating disparities in participation in CRC screening based on

socioeconomic status (Juon et al. 2004, Halliday et al. 2007, Lee et al. 2010). South Koreans

with low income were less likely to participate in screening than individuals with higher

income. The data were consistent with lower screening participation among lower income

Korean Americans, but did not reach statistical significance. A previous study reported that

top two reasons for non-participation in CRC screening among South Koreans were

“without any symptoms” and “lack of time” (Han et al. 2012). Based on these findings, one

may speculate that barriers to screening such as these may be more prevalent among lower

income South Koreans, even though they are eligible for free FOBT from the NCSP. This

highlights the need for health education messages that communicate that CRC screening is

valuable because it detects the disease at an early stage when there are no symptoms.

Previous studies have suggested that one of the most important barriers to cancer screening

for Korean Americans is lack of access to healthcare (Juon et al. 2004). Korean Americans

have the lowest proportion of individuals covered by health insurance and the highest

proportion with no usual source of healthcare among Asian American/Pacific Islanders

(Kagawa-Singer and Pourat 2000). In this study, Korean Americans with health insurance

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were more likely to have received up-to-date CRC screening. Similarly, South Koreans with

private health insurance and higher income had significantly higher odds of participating the

CRC screening despite the existence of a national health insurance system and organized

cancer screening programs such as NCSP targeted to lower income individuals. It is

important to improve the quality of healthcare and access to healthcare services by

expanding health insurance coverage, and factors which are strongly intertwined with

socioeconomic status should be considered as barriers (Sambamoorthi and McAlpine 2003,

Ross et al. 2006). In addition to cost and access to health care, cultural factors and health

beliefs, such as low perceived need for screening in the absence of symptoms, may influence

screening utilization.

This study had limitations. First, no causal relationships were tested to support the

association between the screening rate and incidence/mortality. Second, we were limited to

using each location’s age-standardized incidence and mortality rates as provided by public

data sources; as a result, rates for Koreans in South Korea and for Korean Americans and

non-Hispanic whites in California are standardized to different age distributions and it is

inappropriate to directly compare rates across countries. The standard age distribution of

South Korea is younger than that of the United States, which leads to lower apparent rates.

However, it is valid to compare trends in CRC rates between South Koreans and Korean

Americans in California using these data. Third, both KNHANES and CHIS data are based

on self-report, which could introduce bias. However, other studies have found that self-

reports of CRC screening were reasonably accurate and exhibited no differential bias by

ethnicity (Baier et al. 2000, Walsh et al. 2004). Fourth, KNHANES was administered by in-

person interview whereas CHIS was administered by telephone. The response quality thus

may be different, because of differences in gaining trust and rapport between the

interviewees and interviewers (Holbrook et al. 2003). However, a recent study reported that

the sensitivity and specificity of self-report measures of cancer screening were not different

by survey method (Vernon et al. 2008). Fifth, some questionnaire items in KNHANES and

CHIS (e.g. currently insured) were not identical; therefore, direct comparisons of some

factors associated with participation for CRC screening between South Koreans and Korean

Americans should be done cautiously. Sixth, although one third of all Korean Americans

live in California (Hoeffel et al., 2012), these findings may not be representative of all

Korean Americans.

Despite these limitations, this study provides important comparative information on rates

and trends in CRC–related indices among Korean Americans in California and Koreans in

South Korea. Data suggest that efforts to promote primary and secondary prevention of CRC

in Korean populations are critically important in both countries.

References

Atkin WS, et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicenter randomized controlled trial. Lancet. 2010; 375:1624–1633. [PubMed: 20430429]

Baier M, et al. Validity of self-reported colorectal cancer screening behavior. Cancer Epidemiology, Biomarkers & Prevention. 2000; 9:229–232.

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Appendix

Age-standardized rates of colorectal cancer incidence and mortality among South Koreans

and among Korean Americans and non-Hispanic whites in California, 1999–2009.

South Koreans

Year Incidence, male Incidence, female Mortality, male Mortality, female

1999 27.0 17.1 14.0 8.4

2000 28.1 17.1 14.0 8.4

2001 30.5 18.6 14.8 8.5

2002 33.7 19.6 16.4 9.0

2003 36.0 21.3 16.7 9.4

2004 38.8 22.2 17.1 9.5

2005 42.0 23.8 16.7 9.5

2006 44.2 24.9 16.7 9.3

2007 46.0 25.3 17.4 9.1

2008 47.5 25.8 16.9 9.2

2009 50.2 26.9 16.5 9.1

Korean American in California

Year Incidence, male Incidence, female Mortality, male Mortality, female

1999 43.5 30.5 * 12.4

2000 65.2 34.2 17.4 11.6

2001 45.2 32.3 21.7 14.0

2002 64.2 34.6 18.1 12.7

2003 67.1 29.0 20.3 10.7

2004 46.8 42.9 26.1 14.4

2005 64.1 39.1 20.1 11.8

2006 71.1 39.2 24.1 16.0

2007 59.1 38.4 18.6 11.8

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Korean American in California

Year Incidence, male Incidence, female Mortality, male Mortality, female

2008 60.6 39.1 14.6 9.0

2009 65.8 41.4 19.9 11.6

Non-Hispanic whites in California

Year Incidence, male Incidence, female Mortality, male Mortality, female

1999 62.1 45.3 21.5 15.6

2000 60.7 44.4 21.5 15.6

2001 59.8 43.0 21.8 15.6

2002 57.8 42.2 20.5 15.4

2003 57.3 42.4 21.0 14.7

2004 53.0 39.8 19.9 14.2

2005 52.8 40.0 19.4 13.6

2006 51.9 39.5 18.7 13.2

2007 52.7 39.3 18.5 13.1

2008 50.3 40.2 17.2 13.2

2009 47.8 36.1 17.8 12.8*Statistic not displayed due to fewer than 15 cases.

Sources: The Korea Central Cancer Registry, and Korean Statistical Information Service (1999–2009), California Cancer Registry and CDPH Center for Health Statistics Death Master files 1988–2009. SEER*Stat Database: Asian Mortality-California (1988–2009). Linear interpolation of 1990 and 2000 Census counts for 1988–2009.

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Key Messages

1. Colorectal cancer screening utilization is substantially lower among South

Koreans than among Korean Americans in California.

2. Disparities in colorectal cancer incidence and mortality in both populations are

probably due to an increase in behavioral risk factors and underutilization of

screening.

3. Efforts to promote primary and secondary prevention of colorectal cancer in

Korean populations are critically important in both South Korea and California.

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Figure 1. Trends in age-standardized colorectal cancer incidence and mortality rates among Koreans

in South Korea, and Korean Americans and non-Hispanic whites in California. Sources: The

Korea Central Cancer Registry, and Korean Statistical Information Service (1999–2009),

California Cancer Registry and CDPH Center for Health Statistics Death Master files 1988–

2009. SEER*Stat Database: Asian Mortality-California (1988–2009). Trendlines are from

joinpoint regression modeling. Note: The South Korea and California data were age-

standardized to different age distributions and therefore absolute rates should not be

compared across these two populations.

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Figure 2. Up-to-date CRC screening among South Koreans and Korean Americans in California in

2009.

*Any test includes FOBT within the past year, sigmoidoscopy within the past 5 years, and

colonoscopy within the past 10 years, and DCBE within the past 5 years (only assessed in

the South Korean sample).

# DCBE: Double Contrast Barium Enema

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Table 1

Estimated average annual percent change in colorectal cancer incidence and mortality by population and

gender, 1999–2009

Colorectal cancer incidence

Period AAPC

South Koreans Male 1999–2005 8.1*

2005–2009 4.4*

Korean Americans in California Male 1999–2009 1.8

Non-Hispanic Whites in California Male 1999–2009 −2.5*

South Koreans Female 1999–2006 6.4*

2006–2009 3.0*

Korean Americans in California Female 1999–2009 2.7*

Non-Hispanic Whites in CA Female 1999–2009 −1.7*

Colorectal cancer mortality

Period AAPC

South Koreans Male 1999–2003 5.7*

2003–2009 −0.1

Korean Americans in California Male 1999–2009 −1.3

Non-Hispanic Whites in California Male 1999–2009 −2.5*

South Koreans Female 1999–2004 2.9*

2004–2009 −1.0

Korean Americans in California Female 1999–2009 −1.2

Non-Hispanic Whites in California Female 1999–2009 −2.2*

*Indicates p-value < 0.05

Number and location of joinpoints and average annual percent changes (AAPC) were estimated using the Joinpoint Regression Program Version 4.0.1.

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Table 2

Socio-demographic characteristics of survey participants aged 50 years and older, 2009 Korean National

Health and Nutrition Examination Survey and 2009 California Health Interview Survey

Variables Koreans in South Korea (N=3532)% (SE1)

Korean Americans in California (N=519)% (SE1)

Gender

Male 46.3 (0.8) 38.0 (4.9)

Female 53.7 (0.8) 62.0 (4.9)

Age

50–64 years 61.9 (1.2) 48.9 (5.1)

65 years or older 38.1 (1.2) 51.1 (5.1)

Marital status

Married/living with partner 76.3 (1.1) 78.6 (3.8)

Not married/living with partner 23.7 (1.1) 21.4 (3.8)

Educational attainment

< High school 67.2 (1.6) 16.7 (3.8)

≥ High school graduate 32.8 (1.6) 83.3 (3.8)

Income level (tertile)2

I 52.8 (1.8) 40.8 (4.2)

II 23.4 (1.1) 37.1 (5.5)

III 27.8 (1.6) 22.1 (4.0)

Place of residence

Urban 72.3 (3.1) 97.1 (1.2)

Rural 27.7 (3.1) 2.9 (1.2)

Health insurance

No - 19.6 (2.7)

Yes - 80.4 (2.7)

Private health insurance

No 53.1 (1.3) -

Yes 46.9 (1.3) -

English proficiency

Only/very well/well - 30.0 (4.1)

Not well/not at all - 70.0 (4.1)

Estimates obtained using survey weights.

1SE: standard error

2Income level (tertile) is based on the income distribution within each entire original sample, prior to restrictions on age.

Note: Private health insurance in South Korea generally does not cover CRC screening.

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Tab

le 3

Ass

ocia

tions

bet

wee

n so

cio-

dem

ogra

phic

cha

ract

eris

tics

and

up-t

o-da

te C

RC

scr

eeni

ng a

mon

g K

orea

ns in

Sou

th K

orea

and

Kor

ean

Am

eric

ans

in

Cal

ifor

nia,

200

9 K

orea

n N

atio

nal H

ealth

and

Nut

ritio

n E

xam

inat

ion

Surv

ey a

nd 2

009

Cal

ifor

nia

Hea

lth I

nter

view

Sur

vey

Var

iabl

es

Kor

eans

in S

outh

Kor

ea (

N=3

532)

% (

SE1 )

Kor

ean

Am

eric

ans

in C

alif

orni

a (N

=519

)%

(SE

1 )

Not

scr

eene

dSc

reen

edp-

valu

eN

ot s

cree

ned

Scre

ened

p-va

lue

Gen

der

M

ale

60.5

(1.

7)39

.5 (

1.7)

0.02

31.3

(6.

8)68

.7 (

6.8)

0.15

Fe

mal

e64

.9 (

1.2)

35.1

(1.

2)44

.6 (

7.0)

55.4

(7.

0)

Age

50

–64

58.3

(1.

3)41

.7 (

1.3)

<0.

0001

44.5

(7.

6)55

.5 (

7.6)

0.31

65

+70

.4 (

1.4)

29.6

(1.

4)34

.8 (

6.8)

65.2

(6.

8)

Mar

ital s

tatu

s

M

arri

ed/li

ving

with

par

tner

59.8

(1.

3)40

.2 (

1.3)

<0.

0001

40.0

(7.

6)60

.0 (

7.6)

0.95

N

ot m

arri

ed/li

ving

with

par

tner

72.9

(1.

9)27

.1 (

1.9)

39.4

(6.

5)60

.6 (

6.5)

Edu

catio

nal a

ttain

men

t

<

Hig

h sc

hool

66.1

(1.

3)33

.9 (

1.3)

<0.

0001

36.5

(11

.9)

63.5

(11

.9)

0.77

≥H

igh

scho

ol g

radu

ate

55.5

(2.

2)44

.5 (

2.2)

40.1

(5.

7)59

.8 (

5.7)

Inco

me

leve

l (te

rtile

)2

I

68.6

(1.

4)31

.4 (

1.4)

<0.

0001

43.8

(6.

7)56

.2 (

6.7)

0.69

II

58.7

(2.

2)41

.3 (

2.2)

38.6

(9.

7)61

.4 (

9.7)

II

I54

.0 (

2.1)

45.0

(2.

1)33

.1 (

10.3

)66

.9 (

10.3

)

Plac

e of

res

iden

ce

U

rban

60.8

(1.

3)39

.1 (

1.3)

0.00

438

.9 (

5.4)

61.1

(5.

4)0.

34

R

ural

68.2

(2.

1)31

.8 (

2.1)

60.6

(26

.2)

39.4

(26

.2)

Hav

ing

heal

th in

sura

nce

N

o-

-61

.6 (

9.8)

38.4

(9.

8)0.

007

Y

es-

-34

.2 (

5.4)

65.8

(5.

4)

Priv

ate

heal

th in

sura

nce

N

o70

.3 (

1.5)

29.7

(1.

5)<

0.00

01-

-

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Var

iabl

es

Kor

eans

in S

outh

Kor

ea (

N=3

532)

% (

SE1 )

Kor

ean

Am

eric

ans

in C

alif

orni

a (N

=519

)%

(SE

1 )

Not

scr

eene

dSc

reen

edp-

valu

eN

ot s

cree

ned

Scre

ened

p-va

lue

Y

es56

.3 (

1.5)

43.7

(1.

5)-

-

Eng

lish

prof

icie

ncy

O

nly/

ver

y w

ell/

wel

l-

-31

.6 (

8.1)

68.4

(8.

1)0.

26

N

ot w

ell/

not a

t all

--

43.0

(6.

4)57

.0 (

6.4)

Est

imat

es o

btai

ned

usin

g su

rvey

wei

ghts

.

1 SE: s

tand

ard

erro

r

2 Inco

me

leve

l (te

rtile

) is

bas

ed o

n th

e in

com

e di

stri

butio

n w

ithin

eac

h en

tire

orig

inal

sam

ple,

pri

or to

res

tric

tions

on

age.

Not

e: P

riva

te h

ealth

insu

ranc

e in

Sou

th K

orea

gen

eral

ly d

oes

not c

over

CR

C s

cree

ning

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Table 4

Correlates of up-to-date CRC screening among South Koreans and Korean Americans in California (multiple

logistic regression analysis); 2009 Korean National Health and Nutrition Examination Survey and 2009

California Health Interview Survey

Variables South Koreans Korean Americans in California

Adjusted OR1 (95% CI) Adjusted OR1 (95% CI)

Gender (reference: male)

Female 0.99 (0.83–1.18) 0.73 (0.26–2.04)

Age (reference: 50–64 years)

65 years or older 0.91 (0.74–1.12) 1.05 (0.28–3.95)

Marital status (reference: not married/living with partner)

Married/living with partner 1.48 (1.18–1.85) 1.03 (0.36–2.94)

Educational attainment (reference: <high)

≥ High school 1.16 (0.92–1.47) 0.87 (0.21–3.69)

Income level (tertile) (reference: I)

II 1.22 (0.97–1.52) 1.26 (0.32–5.01)

III 1.34 (1.08–1.66) 1.21 (0.33–4.44)

Place of residence (reference: rural)

Urban 1.21 (0.96–1.51) 3.05 (0.15–62.10)

Having health insurance (reference: no)

Yes - 2.61 (1.04–6.55)

Private health insurance (reference: no)

Yes 1.39 (1.11–1.75) -

English proficiency (reference: well)

Not well/ not at all - 0.74 (0.26–2.09)

Estimates obtained using survey weights.

1All ORs (odds ratios) are adjusted for gender, age, marital status, educational attainment, income level and urban versus rural place of residence.

ORs for South Korean are additionally adjusted for private health insurance status. ORs for Korean American are additionally adjusted for health insurance status and English proficiency. Note: Private health insurance in South Korea generally does not cover CRC screening. Computations conducted using the sample weights provided for each sample.

2Income tertiles are based on the income distribution within each entire original sample, prior to restrictions on age.

Ethn Health. Author manuscript; available in PMC 2015 August 01.